Anthropogenic disturbance is a growing threat, and the physiological consequences of exposure to such stressors is gaining increasing attention. A recent paper published in the Journal of Animal Ecology explores the consequences of stress-relevant hormones for mothers and their offspring. David Ensminger, lead author of the study, is finishing up his PhD with Dr. Tracy Langkilde, taking an integrative approach to examining the role stress-relevant hormones play in allowing an animal to respond to environmental perturbations. Dr. Tracy Langkilde is a Professor and the Head of the Department of Biology at Penn State University, and examines the mechanisms and consequences of population-level responses to global environmental change.
Many animals (including humans) are frequently exposed to stressors. Responses range from behavioral adjustments to escape from or mitigate the stressor, to alterations in the body’s hormonal profile in order to cope with the stressor. One common response is for animals to increase concentrations of “stress” hormones – cortisol in humans and many mammals, and corticosterone in reptiles and birds (hereafter referred to as CORT). In addition to the direct effect of CORT, laboratory experiments on rodents have shown that CORT can have effects that transmit from mothers to their offspring. However, few studies have looked at this phenomenon in wild organisms.
In our recent paper published in the Journal of Animal Ecology, we looked at how elevated CORT in gravid (pregnant) females can affect not only the female herself, but also the eggs she produces and the offspring that hatch out of those eggs. To do this, we collected gravid female fence lizards from the field in southern Alabama. Once back at the lab, we applied CORT to the females’ backs every night, while they were asleep, until they laid their eggs. CORT is commercially available and easily soaks into their skin when mixed with sesame oil, much like moisturizer, causing an elevation in their blood CORT concentrations that mimic the CORT response to natural stressors such as being attacked by fire ants and getting overheated. We applied just sesame oil only to half of the lizards to control for any effect of the oil or our presence.
We tested for effects on the mothers by recording their behavior and taking blood samples to measure blood glucose. We measured the shape of the eggs once they were laid and tested a subsample for hormone and nutrients in the yolk, then incubated the rest of the eggs. Once the hatchlings emerged from the eggs, we took their morphological measurements, recorded their behavior, and took a blood sample for hormone measurements.
We found that this increase in CORT in the mothers while gravid was enough to affect them, their eggs, and their offspring. CORT-treated mothers altered their behavior in ways that may help protect them from predators, including spending less time up on their basking perches where they would be more visible to predators. They also had increased blood glucose 3 days after laying which may give them greater short-term energy reserves. The eggs that the CORT-treated mothers laid were the same size but the makeup of their yolk differed compared to those laid by control mothers: CORT-treated mothers laid eggs that had more CORT and less protein in their yolks. However, offspring that hatched from eggs of CORT-treated mothers were longer from head to tail-tip than those from control mothers. This increase in size was only by 3%, but this could be enough to give them a head-start in the world; similar increases in body length have been shown to increase survival of hatchlings of this and other lizard species. Offspring of CORT-treated mothers had lower levels of CORT in their blood, which may buffer them when they encounter future stressors. They also exhibited increased antipredator-associated behaviors including spending more time hiding and being less likely to break their crypsis (camouflage) when provoked. This could help them avoid and survive predator encounters.
Few previous studies have looked at multiple traits (such as behavior, physiology, and morphology) across different life stages (adult, egg, hatchling), providing only a snapshot of how CORT can alter animals. With this study, we were able to look at transgenerational effects of CORT, from the mother’s behavior and her allocation of hormones and nutrients to her eggs, to effects on behavior, size, and hormones of the resulting offspring. Doing so allowed us to shine a little more light on how CORT alters offspring and potential mechanisms for those changes. The changes we saw could impact the offspring’s ability to survive in the face of stressors such as predators. Stress (CORT) during pregnancy is typically seen as negative, but if these maternal CORT-effects better adapt offspring to a high-stress environment, it could provide evidence that maternal CORT can match offspring to their future environment.
Ensminger, D. C., Langkilde, T. , Owen, D. A., MacLeod, K. J. and Sheriff, M. J. (2018), Maternal stress alters the phenotype of the mother, her eggs, and her offspring in a wild caught lizard. Journal of Animal Ecology. DOI: 10.1111/1365-2656.12891